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10.1146/annurev.ento.50.071803.130337
Annu. Rev. Entomol. 2005. 50:505–28
doi: 10.1146/annurev.ento.50.071803.130337
First published online as a Review in Advance on October 7, 2004
NATURAL HISTORY OF PLAGUE: Perspectives from
More than a Century of Research∗
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Kenneth L. Gage and Michael Y. Kosoy
Bacterial Zoonoses Branch, Division of Vector-Borne Infectious Diseases,
Centers for Disease Control and Prevention, Fort Collins, Colorado 80523;
email: [email protected]; [email protected]
Key Words flea, Siphonaptera, Yersinia pestis, rodent, zoonosis
■ Abstract For more than a century, scientists have investigated the natural history
of plague, a highly fatal disease caused by infection with the gram-negative bacterium
Yersinia pestis. Among their most important discoveries were the zoonotic nature of
the disease and that plague exists in natural cycles involving transmission between
rodent hosts and flea vectors. Other significant findings include those on the evolution
of Y. pestis; geographic variation among plague strains; the dynamics and maintenance
of transmission cycles; mechanisms by which fleas transmit Y. pestis; resistance and
susceptibility among plague hosts; the structure and typology of natural foci; and how
landscape features influence the focality, maintenance, and spread of the disease. The
knowledge gained from these studies is essential for the development of effective
prevention and control strategies.
INTRODUCTION
Plague is a rodent-associated, flea-borne zoonosis caused by the gram-negative
bacterium Yersinia pestis (48, 108, 113). The disease is often fatal in humans, particularly when antimicrobial treatment is delayed or inadequate. Although treatable, plague still causes fear and even mass hysteria, as demonstrated during a
1994 pneumonic plague outbreak in India. Plague’s notoriety comes largely from
its role as the cause of three massive pandemics, including the Black Death, a midfourteenth century calamity that killed nearly one third of Europe’s population and
remains the standard by which the effects of AIDS, SARS, or other new diseases
are measured.
The perception that plague is only of historical interest has changed somewhat
because of media reports that suggest Y. pestis could be a weapon of bioterrorism
(70). Often lost in these messages, however, is that since the last pandemic began in
*The U.S. Government has the right to retain a nonexclusive, royalty-free license in and to
any copyright covering this paper.
505
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the late 1800s, plague’s geographic range has expanded greatly, posing new threats
in previously unaffected regions, including the western United States, portions of
South America, southern Africa, and Madagascar, and certain regions of India
and Southeast Asia (34, 48, 113) (Figure 1). Epidemics still occur frequently in
developing countries where plague is endemic and persons live in unsanitary, ratinfested environments. Between 1987 and 2001, outbreaks involving hundreds of
cases occurred in at least 14 countries, usually as a result of exposures to infectious
rat fleas (143). From 1994 to 2003, only 61 cases (7 fatal) in the United States
were identified (Centers for Disease Control, unpublished data). These cases and
others in recent decades were acquired through exposures to wild rodent flea bites
or handling infected mammals, including rodents, rabbits, wild carnivores, and
domestic cats (48–52, 93).
Wildlife biologists have increasingly realized that certain wild mammal species
also are highly susceptible to plague, a fact that can hamper recovery efforts for
species such as prairie dogs or black-footed ferrets (17, 18). The black-footed ferret (Mustela nigripes), a highly endangered predator, is placed in double jeopardy
because it preys almost entirely on prairie dogs and is itself highly susceptible to
plague.
This article provides a selective review of research on plague and its natural
history since Yersin’s initial discovery of the plague bacillus in 1894. Because of
space limitations, many topics, including most medical, microbiological, and public health aspects of plague, are neglected. Fortunately, these have been addressed
in other reviews (5, 6, 10, 20, 23, 26, 34–36, 48–51, 60, 70, 93, 108, 111–114, 135).
THE BASIC TRANSMISSION CYCLE
Y. pestis is maintained in nature through transmission between hematophagous
adult fleas and certain rodent hosts, with occasional involvement of some lagomorphs (48, 115) (Figure 2). Evidence of Y. pestis infection also has been identified
among the Artiodactyla, Carnivora, Hyracoidea, Insectivora, Marsupialia, and Primates, which suggests that virtually all mammals can become infected with this
agent (48, 49, 115). Susceptibility among these nonrodent, nonlagomorph species
varies widely, but all are considered incidental hosts of plague, except perhaps the
house or musk shrew (Suncus murinus) in Southeast Asia and Madagascar. Birds,
reptiles, and amphibians are generally thought to be resistant to Y. pestis infection.
Mammals or birds that prey on plague hosts might play an indirect role in the
spread of plague by moving infectious fleas between areas (52).
Typically, plague is thought to exist indefinitely in so-called enzootic (maintenance) cycles that cause little obvious host mortality and involve transmission between partially resistant rodents (enzootic or maintenance hosts) and their
fleas (51, 111, 112) (Figure 2). Occasionally, the disease spreads from enzootic
hosts to more highly susceptible animals, termed epizootic or amplifying hosts,
often causing rapidly spreading die-offs (epizootics). Although these concepts
seem reasonable, the evidence for separate enzootic and epizootic cycles is often
unconvincing, and epizootics might simply represent periods of greatly increased
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NATURAL HISTORY OF PLAGUE
Distribution of plague foci and countries reporting plague.
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Natural cycles of plague.
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transmission among the same hosts and fleas that support Y. pestis infection during
interepizootic periods.
Understanding the factors that lead to epizootics is important because it is during
these events that the disease spreads rapidly. Humans and other highly susceptible
mammals also experience their greatest exposure risks during epizootics. Recent
modeling studies have suggested that the abundance of susceptible hosts must
exceed certain limits for plague to invade and persist in new areas (32a). Climatic
factors appear to be important in many but perhaps not all areas (24, 25, 41, 44, 105,
113, 129). Recently, a trophic cascade hypothesis was proposed whereby increased
precipitation results in greater plant growth and rodent food production, leading to
increased host populations and a greater likelihood of epizootics and human cases
(105). Others developed models that incorporated temperature and precipitation
effects and noted that increased precipitation likely leads to increased host and
flea populations and heightened plague risk, whereas high threshold temperature
(>32.2–35◦ C) values should decrease flea survival and lower this risk (44). Some
have proposed that epizootic activity decreases during hot weather (≥27.5◦ C)
because high temperatures adversely affect blockage of fleas by Y. pestis (24).
Different factors purportedly influence the dynamics of enzootic plague cycles
through their effects on interactions between Y. pestis and its hosts and vectors
(7, 87). These factors include heterogeneity among Y. pestis strains, density and
diversity of rodent communities, host immune status, genetic structure of host populations, physiologic status of hosts or vectors, species of flea vector, mechanisms
of transmission, mutagenic effects of phagocytic cells on Y. pestis, bacteriophage
activity, and interactions between Y. pestis and other bacteria, (3, 7, 45, 48, 71, 87,
102, 104, 115).
THE PLAGUE BACTERIUM
Y. pestis is a gram-negative coccobacillus that belongs to the Enterobacteriaceae, a
family that includes Escherichia coli, Salmonella typhi, and other enteric pathogens
typically transmitted through contaminated food and water (108). Among the Enterobacteriaceae, Y. pestis is unique in both its choice of host habitat (blood,
lymphoid system, reticuloendothelial system) and primary mode of transmission
(flea vectors). To exist as a vector-borne pathogen, the plague bacterium must
not only survive in its vertebrate host, but also disseminate from the site of inoculation, usually a flea bite, and proliferate, causing a high bacteremia that can
serve as a source of infection for feeding fleas (5, 22, 43). Dispersal of Y. pestis
within the host is enhanced by a plasminogen activator (Pla) that has fibrinolytic
activity (108). Other virulence factors include an array of Yersinia outer proteins
(Yops) and the pH 6 antigen, which are involved in cytotoxic processes, immune
suppression, or survival of Y. pestis within naı̈ve host phagocytes in the initial
stages of infection. Upon exiting the vector and entering the higher-temperature
environment of the vertebrate host, Y. pestis begins to express the F1 capsular
antigen (Caf1), thereby enabling it to resist phagocytosis and killing by potentially
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activated monocytes later in the course of infection. The yersiniabactin siderophore
system and other iron uptake systems enable Y. pestis to acquire this essential
nutrient in blood or other environments where its availability is limited by host
iron-binding molecules (107). Rough Y. pestis lipopolysaccharides probably confer resistance to compliment mediated lysis. Y. pestis endotoxin also presumably
causes the signs and symptoms associated with septic shock, systemic inflammatory response syndrome, and other serious conditions likely to cause death (36,
108, 111). Two additional virulence factors, murine toxin (Ymt) and the pgm locus, not only are associated with pathogenicity in mammals but also affect the
survival of Y. pestis in fleas (Ymt) or its transmission by these vectors (pgm locus) (63, 64). The pgm locus consists of two linked regions (107). The first is a
high pathogenicity island that bears the genes for the yersiniabactin siderophore
system (see above), and the other, which is called the hms locus, contains genes
required for Y. pestis to bind hemin or Congo red (pigmented phenotype) and form
blockages in the foreguts of vector fleas.
Although the closely related Y. pseudotuberculosis can survive for relatively
long periods in water or soils, most researchers believe the plague bacterium perishes quickly outside its normal hosts or vectors (20, 108). Nevertheless, some have
reported that Y. pestis can survive for many days to weeks in flea feces, tissues
of dead animals, and a few other naturally occurring substrates, including soils.
Survival in soils has been proposed as a possible mechanism for plague persistence
during interepizootic periods (9, 98). According to this scenario, Y. pestis cycles
between a short and unstable parasitic phase associated with rodents and fleas and
a more stable soil (saprophytic) phase that allows for survival between epizootics
(9). Others have proposed that Y. pestis might survive as an intracellular parasite
of soil protozoa (38, 103, 117) or exist in a latent (nonculturable) form in soils
(131). Some have even speculated that Y. pestis might undergo prolonged survival
in plants (94, 124). If plague bacteria do indeed survive in soils, soil protozoans,
or plants, rodents presumably could reacquire infection while burrowing or foraging. Although such hypotheses deserve further investigation, they do not seem, at
least at first glance, to agree with observed patterns of transmission and have been
received with much skepticism.
EVOLUTION OF PLAGUE
Early concepts about plague evolution concentrated on the types and distribution
of hosts utilized by Y. pestis. Kucheruk (89, 90) concluded that the origin of
plague coincided most closely with the appearance of burrow-dwelling rodents that
were abundant in dry unwooded steppe and desert regions. Contrary to previous
opinions, he decided that Rattus spp. were important only in secondary foci that
arose as a result of human activity and therefore played no role in the early evolution
of Y. pestis. He also noted that although other murids, along with sciurids and
caviids, were important hosts in some foci, the distribution of plague in Eurasia,
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Indo-Malaya, Africa, and the Americas corresponded closely only with that of
the Cricetidae, a group that included gerbillines, microtines, sigmodontines, and
cricetines. Notably, cricetids represented 82 of 183 mammalian species reported to
be naturally infected with Y. pestis. On the basis of these observations, Kucheruk
concluded that plague first evolved in the Cricetidae, perhaps appearing during
the Oligocene (23–38 mya)–Miocene (5–23 mya) era, with the upper Oligocene
or lower Miocene periods considered most likely. North America and Eurasia
were considered likely sites of origin for plague, although the Cricetidae probably
originated in northern Asia. Historical evidence also indicates that plague was
first introduced into North America around 1900, when rat-infested ships brought
the disease from Asia, a finding that is supported by molecular studies indicating
that plague strains from this continent are similar to others identified from areas
affected by the last pandemic (48, 59, 113). Most evidence suggests plague arose in
Asia, although Y. pestis has been present in east-central Africa for most of the past
two millennia and probably longer. Recently, Suntsov & Suntsova (132) proposed
an alternative hypothesis for the evolution of plague that involves marmots, their
hibernation behaviors, and larval parasitism by one of their fleas.
Kucheruk and others probably were mistaken in their belief that plague arose
many millions of years ago. DNA-DNA hybridization assays and sequencing of
the 16S rRNA gene indicate a close relationship between Y. pestis and Y. pseudotuberculosis (14, 136). The chromosomal DNA of these bacteria are similar and
have an approximately 70-kb plasmid (pLcr) that carries genes for Yops found in
both species (20, 108). Recently, Achtman et al. (1) analyzed 6 genes from each of
the 36 plague strains that were selected to include representatives from each of the
three plague biotypes. Their results suggested that Y. pestis is a recently evolved
clone of Y. pseudotuberculosis, appearing as recently as 1500 to 20,000 years ago.
Considering their genetic similarity, the marked differences in pathogenicity between Y. pestis and Y. pseudotuberculosis are striking. The most obvious genetic
differences are two plasmids (pPCP1 and pFra, also called pMT in some strains)
found in Y. pestis but absent in Y. pseudotuberculosis (108). pPCP1 contains the
plasminogen activator noted above, a bacteriocin (pesticin), and a pesticin immunity protein; pFra contains the genes for Ymt and the fraction 1 capsular antigen
(Caf1). The origins of these plasmids remain uncertain but approximately 50%
of the Y. pestis pFra (or pMT) DNA sequences share a high degree of similarity
(over 90% of the similar regions exhibited >96% DNA identity) to those on a
Salmonella enterica serovar typhi plasmid (116).
CLASSIFICATION OF STRAINS AND THEIR
ASSOCIATION WITH MAMMALIAN HOSTS
Variation among Y. pestis strains is associated with geographic origins, host associations, virulence, or possible links to past epidemics, including the three great
pandemics (6, 37, 56, 59, 86). Unlike many bacterial pathogens, Y. pestis has only
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one serotype, but typing schemes have been developed on the basis of variations in
biochemical reactivity for certain substrates, primary host associations, ribotypes,
and other molecular markers (2, 59, 68, 82, 99).
Expanding on earlier work by Berlin & Borzenkov (15), Devignat (37) identified
three Y. pestis biotypes (antiqua, mediaevalis, and orientalis) that differed in their
abilities to acidify glycerol and reduce nitrates. The distributions of these biotypes
corresponded reasonably well with the sites of origin and areas affected by the three
pandemics [Justinian’s Plague, Black Death, and Modern (Third) Pandemic]. Later
ribotyping studies provided support for Devignat’s scheme (59).
Tumanskii (137, 138) proposed three host-related Y. pestis varieties: ratti (ratborne), marmotae (marmot-borne), and citelli (suslik-borne), and Levi (92) identified another vole-specific variety (microti). Stepanov (130) later suggested that
these varieties should be recognized as Y. pestis subspecies because of their specific characteristics, geographic distributions, adaptations to particular rodents, and
level of virulence for animals, a proposal that was further modified by Kozlov (86),
who listed biochemical reactivities and virulence characteristics that distinguished
separate biotypes among Stepanov’s subspecies. Recently, Gorschkov et al. (56)
used a DNA probe to fingerprint 85 Y. pestis strains from different natural foci.
The seven genetic variants identified were associated with certain rodent species
and geographic regions. Although the above studies indicate that Y. pestis strains
vary among regions in a manner that correlates well with the predominant host
found in each region, it is not clear whether these correlations represent evidence
of adaptation of the strains to these host species or simply geographic variation
that has arisen over time.
In China, investigators identified 17 distinct Y. pestis types on the basis of
variations in biochemical properties, nutritional requirements, virulence factor expression, and other features (95). Additional studies documented variations among
plasmid profiles and ribotypes of Chinese strains, including one that describes an
interesting 6-kb plasmid of uncertain function and origin (39). Y. pestis strains
bearing this plasmid have been spreading among rats and fleas in southwestern
China, where the last pandemic arose.
North American strains of Y. pestis are less diverse than those found in Asia,
which is hardly surprising considering that only a limited number of orientalis
biotype strains were likely to have been introduced into this continent during the
last pandemic. Interestingly, plague strains from North America have a distinctive
19-kb dimer of the 9.5-kb plasmid (pPCP1) that does not appear in other orientalis
isolates collected from various areas affected by the above pandemic (27). Recently,
multiple-locus variable number tandem repeat analysis, PCR-based IS100 genotyping, and pulsed-field gel electrophoresis have been used to analyze variation
among North American and other strains (2, 68, 82, 99). The above methodologies
are still under evaluation but undoubtedly will be useful for epidemiological and
ecological studies, as demonstrated in a study that investigated Y. pestis population
genetic structure and transmission patterns during an epizootic in prairie dogs in
Arizona (54a).
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MAJOR MAMMALIAN HOSTS OF PLAGUE
Among the 203 rodent species or subspecies and 14 lagomorph species reported
to be naturally infected with Y. pestis (114), only a small proportion are actually
significant hosts. Although certain lagomorphs, such as pikas in central Asia,
appear to be important, rodents are the major host taxon (48, 57). Each of these
small mammals possesses unique characteristics that influence its ability to serve
as a host of plague, although most have certain features in common. Many members
of important host populations, probably 40% or more, not only become infected
with Y. pestis but also circulate sufficient numbers of bacteria in their blood (>106
Y. pestis ml−1 blood) to serve as reliable sources of infection for feeding fleas (22,
43, 115). Few, if any, hosts that become so heavily bacteremic survive, but more
resistant members of the same population might develop less severe illness and live
to reproduce. Major plague hosts also are often heavily infested with one or more
important flea vectors, a trait that obviously promotes the spread of the disease.
Finally, many significant hosts live in burrows that support large flea populations,
and those that dwell elsewhere, such as wood rats (Neotoma spp.), often have
complex nests that are also heavily flea infested (101, 106, 111).
RESISTANCE TO PLAGUE IN MAMMALIAN
HOST POPULATIONS
Host susceptibility to Y. pestis–induced mortality depends on many factors, including host species, genetic differences among individuals and populations, age,
breeding status, immune and physiologic status, and season of the year (69, 85,
115). Allegedly resistant host populations typically consist of a mixture of highly
susceptible individuals that usually die following infection and more resistant animals that become infected but eventually recover, as indicated by the detection
of specific antibodies or resolving Y. pestis lesions in their tissues (49, 79, 113).
Although the evidence is limited, some researchers have proposed that recovered
hosts might become chronic carriers of plague, thereby acting as reservoirs for
maintaining the disease between transmission seasons or epizootics (113, 141,
142). Others believe that normally susceptible animals might become infected
shortly before entering hibernation, maintain a latent infection while hibernating,
and then succumb to plague upon reawakening in the spring (54, 115).
Species that exhibit heterogeneous responses to infection include gerbils (Meriones spp. and Rhombomys opimus) and marmots in Asia (Marmota spp.), and
deer mice (Peromyscus maniculatus) and California voles (Microtus californicus) in North America (51, 79, 86, 110–112). Certain other hosts are more susceptible and typically undergo devastating die-offs when infected with Y. pestis.
Black-tailed prairie dogs (Cynomys ludovicianus) experience almost 100% mortality during epizootics (17, 18, 111), and other sciurid species, including other
prairie dog species, are nearly as susceptible (18, 30, 88, 121, 134). Recent
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evidence suggests that plague not only causes high mortality among prairie dogs
but also reduces genetic variability within their populations (136a).
The occurrence of significant resistance among a rodent population might indicate past contact with plague and selection for resistant individuals (47, 96, 113,
115, 122), and some have proposed that the only true hosts of plague are those that
have survived repeated contact with the disease. It has been further suggested that
the role a particular host population plays in maintaining plague is determined by
the ratio of resistant (survives infection) to susceptible (dies following infection)
individuals within that population. The great gerbil (R. opimus) was considered
the most important host in central Asian desert foci because 40% to 60% were
resistant to Y. pestis–induced mortality, a level higher than that observed for other
sympatric gerbils of the genus Meriones (110, 123). Some Asian marmots, including certain populations of Marmota sibirica, also exhibit relatively high resistance
(54). In other instances no particular host stands out as unusually resistant. For
example, resistance in the Ural steppe focus of Kazakhstan was about equal for
great gerbils (50%–80%), little susliks (Spermophilus pygmaeus) (50%–70%), and
midday gerbils (Meriones meridianus) (44%–60%) (7).
Relatively few studies have addressed resistance among North American rodents. Thomas et al. (133) compared Y. pestis infections in northern grasshopper
mice (Onychomys leucogaster) collected from a plague-free area in Oklahoma
with those from a plague-affected region of Colorado and found that the plaguenaı̈ve mice were much less resistant than the Colorado population. Variations in
plague resistance among populations of deer mice (P. maniculatus) and California voles (M. californicus) also have been reported (119, 120), and this resistance
is known to be genetic in M. californicus (69). Kangaroo rats (Dipodomys spp.)
are considered highly resistant (67). Although some studies suggest that repeated
plague exposures result in the appearance of at least partial resistance among rodents, populations of California ground squirrels (Spermophilus beecheyi), rock
squirrels (S. variegatus), and prairie dogs (Cynomys spp.) have remained highly
susceptible (111, 112, 121, 131), and epizootics still cause high mortality among
some suslik populations (Spermophilus spp.) in Asia (88).
TRANSMISSION OF YERSINIA PESTIS BY FLEAS
In 1897 Ogata (113) suggested that fleas might transmit Y. pestis, and succeeded
in infecting mice by injecting them with ground suspensions prepared from fleas
that had fed on infected rats. One year later Simond demonstrated that rat fleas
previously fed on infected rats could transmit Y. pestis to uninfected rats. In
1913 Swellengrebel demonstrated that transmission by Xenopsylla cheopis occurs through the rat flea’s mouthparts rather than through contamination of the
feeding site with infectious flea feces.
A classic study by Bacot & Martin (8) describes the development of Y. pestis
infections in X. cheopis and the blocking process that enables these fleas to be efficient vectors. They found that after X. cheopis feeds on an infected rat, the ingested
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plague bacteria multiply rapidly in the flea’s midgut and spine-filled proventriculus and form noticeable colonies in just a few days. As these colonies grow and
coalesce, they eventually become large enough to occlude the proventriculus, effectively blocking the movement of blood from the foregut to the midgut, causing
the flea to starve. Blocked and starving fleas repeatedly attempt to feed by using
their pharyngeal muscles to draw blood into the foregut, which causes distension of the esophagus but no movement of blood past the proventricular block.
Eventually the flea is forced to relax its pharyngeal muscles, which results in
Y. pestis–contaminated blood being flushed from the distended esophagus back
into the feeding site, thereby causing infection of the vertebrate host.
Many factors influence blocking and transmission, including Y. pestis strain
differences and transmission factors, flea species, proventricular morphology, and
temperature (16, 22, 24, 32, 43, 46, 60, 61, 63, 64, 71a, 73, 75, 76, 79, 115). The
ability of Y. pestis to form blockages in fleas is associated with its ability to bind
Congo red (CR) or absorb exogenous hemin when grown on media containing these
compounds (16, 108). Strains that fail to bind hemin or CR are less “sticky” than
pigment-positive strains, which provides a likely explanation for their inability to
form blocks. To bind hemin or CR, Y. pestis must possess a group of chromosomal
genes called the hemin storage (hms) locus. Hinnebusch et al. (63) demonstrated
that a Y. pestis hms mutant containing a deletion in the hmsR gene of the hmsHFR
region of the hms locus was incapable of forming blocks in fleas, as was a polar
mutant with a single transposon insertion in hmsH. The ability of both mutant
strains to cause blockages could be restored by complementing the bacteria with
a plasmid that bears functional hmsHFR genes.
If fleas are to become blocked, Y. pestis must grow in their guts. Hinnebusch
et al. demonstrated that for Y. pestis to colonize the flea midgut, the 110-kb plasmid
(pMT or pFra) must be present and express murine toxin (Ymt) (61, 64). Others
have suggested that the ability of Y. pestis to form biofilms in flea guts might
be critical for colonization and blocking (31, 71a). The fleas themselves also
must provide a suitable environment for Y. pestis growth. Engelthaler et al. (43)
compared Y. pestis infections in X. cheopis and Oropsylla montana and found that
early in the course of infection Y. pestis colonies often appeared simultaneously in
the proventriculus and midgut of X. cheopis, but only in the midguts of O. montana.
This could explain why the latter requires much longer blocking times, has lower
blocking rates, clears itself of infection more frequently, and is generally a much
less efficient vector than X. cheopis (22, 43, 65).
Differences in blocking rates also might be explained by the structure of the
proventriculus (46). It was reported that blocking in Citellophilus tesquorum occurred in those fleas that had high levels of fluctuating asymmetry among their
proventricular spines (84). Strictly morphological explanations, however, are unlikely to explain why certain flea species not only fail to become blocked but also
are highly resistant to Y. pestis colonization in their guts.
Temperature obviously affects transmission (24, 44, 113). Block formation
in two rodent fleas, C. tesquorum and Neopsylla setosa, was optimal at 16 to
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22◦ C (58). Blocking rates and times differed between these fleas, however, with
53.3% to 55.1% of N. setosa becoming blocked within 3 to 4 days after taking an
infectious blood meal, whereas 10 to 14 days were required for 28.0% to 42.7% of
C. tesquorum to do so. Interestingly, blocking in C. tesquorum depended mainly
on the frequency of feeding, whereas duration of feeding was more important
in N. setosa. Cavanaugh (24) reported that infected fleas held at temperatures
above 27.5◦ C had decreased transmission rates compared with those held at lower
temperatures. Kartman (74) noted that clearance of infection increased more than
10-fold and blocking rates decreased by slightly more than half for X. cheopis held
at 29.5◦ C rather than 23.5◦ C. These effects were attributed to the temperaturedependent fibrinolytic activities of the Y. pestis plasminogen activator (Pla) (24), a
hypothesis that was later refuted by Hinnebusch et al. (61), who found that blocking
rates decreased with temperature even among fleas that had been infected with
Y. pestis strains lacking the plasmid (pPCP) that carries the gene for Pla.
Compared with most other fleas, X. cheopis is an unusually effective and dangerous vector, particularly in plague-endemic areas that are heavily rat infested.
This flea is remarkable in its ability to become blocked, and therefore infectious,
within as few as 5 days after imbibing Y. pestis–infected blood (46). Other common
rat fleas, with the probable exception of Xenopsylla brasiliensis, are less effective
vectors. X. astia, a flea that occurs in southern Asia, is a relatively inefficient transmitter of plague, which suggests that phylogenetic relationships among vectors
are an unreliable indicator of likely vector competency (113). The northern rat
flea, Nosopsyllus fasciatus, also transmits Y. pestis but much less efficiently than
X. cheopis. Although it is generally accepted that wild rodent fleas are important
vectors of Y. pestis, they typically transmit at lower rates than X. cheopis (22, 43,
46, 65, 66, 113). Some even clear themselves of infection soon after ingesting a
presumably infectious blood meal (40, 46). Other wild rodent fleas support Y. pestis
infections in their midguts but fail to become blocked, or do so only rarely, while
others become blocked only after extrinsic incubation periods of many weeks to
a few months. Recently developed quantitative competitive PCR techniques can
be used to estimate the numbers of Y. pestis found in field-collected fleas, thereby
providing useful information on whether individual fleas are likely to be blocked
or merely infected (42, 62).
The roles played by most wild rodent fleas in plague transmission are poorly
known (111). The number of potential vectors is great (114). Serzhan & Ageyev
(127) analyzed a list prepared by Goncharov of 263 fleas reported to be naturally
infected with Y. pestis and found that 223 of these (85%) were specific parasites of
rodents and 145 (55.0%) were further specific for cricetids. Most of the infected
fleas (57%) came from the Palearctic region, 22.9% occurred in North America, and
the remainder originated from foci in southern Asia, Africa, and South America.
Despite the large number of species potentially involved, only those fleas that are
found on key hosts and able to transmit under natural circumstances are likely to
be important.
That many wild rodent fleas are considered important vectors but block at
much lower rates than X. cheopis raises interesting questions about the relative
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roles of blocked, partially blocked, and infected but completely unblocked fleas
in the transmission of plague. Relatively little data exist on this subject, but some
researchers have reported experimental transmission by infected and unblocked
or partially blocked fleas (13, 22, 33, 53, 140). In separate studies, individual,
block-free O. montana succeeded in transmitting Y. pestis four days after feeding
on infectious hosts (22, 43). Despite being an important vector in southern Siberia,
the suslik flea C. tesquorum altaicus blocked at low rates (5.8%), an apparent
discrepancy that could be explained by the fact that 40% to 50% of infected
but block-free fleas experimentally transmitted Y. pestis to susceptible animals
(13, 140). Similarly, infected Rhadinopsylla rothschildi and Rh. daurica exhibited
low blocking rates (2.1%–12.5% and 7.2%–10.5%, respectively), but block-free
individuals of both species succeeded in transmitting Y. pestis to Microtus brandti
and to Spermophilus daurica (53). In yet another study, Degtyareva et al. (33)
reported that block-free fleas from the Dagestan alpine focus could transmit plague
to common voles.
The importance of mechanical transmission also should be further investigated.
Bibikova (16) discounted its importance, noting that Y. pestis survived for only 3 h
on flea mouthparts. Others, however, have taken a more moderate view. Kartman
et al. (76, 77) and Burroughs (22) suggested that transmission by blocked vectors
is important in enzootic cycles and that mechanical transmission is most significant during epizootics. Indeed, such transmission might explain how die-offs can
spread so rapidly among prairie dogs, ground squirrels, and other highly susceptible
species that harbor fleas that apparently take weeks to months to become blocked.
Although the mouse and vole flea Malaraeus telchinum rarely becomes blocked, it
can transmit plague when large numbers of fleas are placed on susceptible animals
soon after they have taken an infectious blood meal, a finding strongly suggestive
of mechanical transmission (21, 22, 77). Another sympatric flea, Hystrichopsylla
linsdalei, was far less abundant than M. telchinum but blocked efficiently and was
thought to be important in enzootic transmission of Y. pestis (76). Others have suggested that even X. cheopis might transmit mechanically during plague epizootics
(118). Pulex irritans is an exceptionally poor biological vector of plague but can
transmit the disease mechanically, a fact that may explain why some regions in
developing countries, or perhaps parts of Europe during the Black Death, suffered
outbreaks of bubonic plague in the apparent absence of X. cheopis (19).
The ability to experimentally transmit Y. pestis is likely to provide some indication of whether a particular flea species will be an important vector; however, other
factors must be considered. Fleas that are highly host specific might be suitable
vectors for transmitting plague among a particular host species but are less likely to
spread the infection to other species. Otherwise suitable vectors might also occur
in plague-free regions or appear as adults during a time of the year when few host
animals are bacteremic, making it unlikely that these fleas will become infected
and transmit plague. The ability of Y. pestis–infected fleas to survive in off-host
environments should also be considered, as this provides a means for maintaining
Y. pestis over extended periods, including from one transmission season to the
next.
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FLEAS AS RESERVOIRS OF YERSINIA PESTIS
Although fleas often die relatively quickly after becoming blocked, infected but
unblocked fleas, and occasionally even blocked fleas, can survive for many months.
Infected Ctenophthalmus breviatus, C. tesquorum, and N. setosa survived for up
to 220 days when held at 14 to 27◦ C and Ct. breviatus survived for 396 days at
0 to 15◦ C (55). In another experiment, more than half the C. tesquorum altaicus that
fed on infected long-tailed susliks (Spermophilus undulatus) maintained Y. pestis
from mid-September to mid-June, thus allowing the plague bacterium to survive
during hibernation of their hosts (11). A few fleas (0.7% to 19.4%) survived from
one summer to the next and 30% of these remained infected. A single female
survived through two winters and lived for 411 days after feeding on an infected
suslik. Most importantly, infected fleas that survived through the winter transmitted
plague to healthy susliks. In a field study, Sharets et al. (128) plugged the openings
of marmot burrows and found that infected Rhadinopsylla li ventricosa were still
present after nearly 14 months. Infected prairie dog fleas (Oropsylla labis and
O. tuberculata cynomuris) also were recovered from burrows in Colorado for
more than one year after their hosts had perished from plague (78).
CHARACTERIZING PLAGUE FOCI AND HOSTS
Zabolotny (144) proposed that the 1910–1911 Manchurian epidemic, which killed
50,000 to 60,000 people, was caused not by the introduction of plague through
movement of infected rats or people, but rather by a spillover of infection from a
natural focus that existed in native marmots. Zabolotny’s recognition of the link
between this human outbreak and disease observed among marmots represents
one of the first discussions of a natural plague focus. Since that time many authors
have proposed various concepts on the hosts, landscape characteristics, structure,
and typology of these foci.
PRIMARY AND SECONDARY HOSTS
Fenyuk (47) proposed classifying hosts as either primary or secondary carriers of
plague. According to this concept, primary hosts and their fleas maintain plague in
natural foci without the involvement of other potential hosts. Conversely, secondary
hosts and their fleas cannot maintain Y. pestis in the absence of primary hosts but
might assist in disseminating the disesase. Rall (122) later proposed that the ability
of an animal to act as a primary host depends on its susceptibility, abundance,
distribution, and behavior. Other proposed factors include coloniality, proximity
of colonies to one another, use of complex burrow systems, resistance to a specific
biotype of Y. pestis, ability of resistant animals to produce high antibody titers
and levels of phagocytic activity, and occurrence of prolonged bacteremias in
susceptible animals (B. Suleimenov & N. Klassovskii, personal communication).
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Opinions differ on whether a single primary host and its fleas actually can
maintain plague within a focus without the involvement of other hosts. Rall (122)
believed that this was indeed true in central Asia and supported the related concept
of monohostality (72), wherein Y. pestis can be maintained in a particular focus
through infection of a single host, such as the great gerbil (R. opimus) in central
Asian desert foci. Other investigators (72, 100) believed that these foci are supported by multiple hosts (polyhostality). Siberian susliks (S. undulatus) and Pallas’
pikas (Ochotona pallasi) were considered important in the same Mongolian focus, as were Daurian susliks (S. dauricus) and rats (Rattus spp.) in northeastern
China; Siberian marmots (Marmota sibirica), Daurian susliks (S. dauricus), pikas
(Ochotona spp.), and voles (Microtus spp.) in the Daurian enzootic area; and little
susliks (Spermophilus pygmaeus), gerbils, and jerboas in central Asia. Although
Petrov (109) and many others proposed that the great gerbil and its fleas support
monohostal foci in the deserts of central Asia, others believed that maintenance in
these areas depends on the presence of additional rodent species. In the foothills
of Kopet-Dag, Mangishlack, and western and northwestern Turkmenia, R. opimus
and the Libyan jird (Meriones libycus) were considered essential for maintaining
plague, whereas R. opimus was joined by the midday gerbil (M. meridianus) in
the Aral Karakum and northwestern Kizilkum deserts, the little suslik north of
the Aral Sea, and the Aral yellow suslik (Spermophilus fulvus) on the Krasnovodsky Peninsula (91). One of the most interesting questions is whether commensal
rats can maintain plague in the absence of other rodent hosts. Although some
have doubted whether this is possible, Y. pestis circulates for decades in some
areas without the apparent involvement of other hosts (115), and rats are considered the primary hosts of plague in Vietnam and Madagascar (57). Recent
modeling studies have suggested that plague can persist in small rat subpopulations for indefinite periods and serve as sources of infection for later outbreaks
(80, 81).
The concepts of primary and secondary hosts, as well as monohostality and
polyhostality, have not appeared extensively in the American literature. Instead,
important rodent species have been characterized as enzootic (maintenance) or
epizootic (amplifying) hosts (111, 112). According to this scheme, plague is maintained primarily in so-called enzootic cycles that involve transmission among presumed enzootic hosts, namely various species of Peromyscus and Microtus, and
their fleas. As noted above, Y. pestis is believed to occasionally spread from its enzootic hosts to other highly susceptible epizootic hosts, often causing widespread
die-offs among these animals. Commonly proposed epizootic hosts include various
prairie dogs, ground squirrels, chipmunks, and wood rats.
Although the occurrence of epizootic cycles is suggested by obvious die-offs
among presumed epizootic hosts, little evidence exists to indicate that supposed
enzootic hosts (Peromyscus spp. and Microtus spp.) are truly essential for the
interepizootic maintenance of plague. Alternatively, plague might be maintained
during interepizootic periods through low-level transmission among a number of
potential host species and their fleas, causing epizootics only when environmental
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conditions are favorable and host populations are high. The long-term maintenance
of plague in such a polyhostal system would be favored not only by the presence
of multiple host and flea species but also by the patchy distribution of these hosts
within multiple habitats, thus ensuring that all populations of these animals are
never completely wiped out and that low levels of transmission can occur as plague
slowly passes from patch to patch and as host populations recover from previous
epizootics. Pollitzer & Meyer (115) also cautioned that the importance of supposedly resistant hosts, such as P. maniculatus, for maintaining plague foci between
epizootics might be overrated, noting that various mechanisms in addition to spatial isolation could ensure plague persistence even among highly susceptible host
populations, including age-related or seasonal variations in susceptibility and the
possibility that hosts could maintain latent infections while hibernating and thus
carry Y. pestis from one transmission season to the next.
TYPOLOGY OF PLAGUE ENZOOTIC TERRITORY
Several scientists developed systems for typing natural plague foci in the former
Soviet Union, China, and neighboring regions (89, 109, 122). Kucheruk (89) proposed five types of plague foci for the Palearctic region on the basis of primary
mammalian hosts, flea vectors, Y. pestis biotypes, and landscape characteristics.
These included a suslik type in the steppes of the Pre-Caspian Sea region, central Caucasus mountains, Transbaikalia, and northeastern China; a marmot type
in meadow belts of the Gissarski Hrebet, Alaj, and Pamir mountains; a pika type
in the steppe belt of the Altay mountains; a vole alpine type in the Caucasus and
Gissarski Hrebet mountains; and a gerbil type spread across the vast deserts that
occur from the western Sahara to the eastern Gobi. Chinese scientists also developed a system for typing plague foci on the basis of the occurrence of particular
landscapes, the presence and characteristics of principal hosts and fleas, and the
existence of Y. pestis infections in these same hosts and fleas (95).
In North America, Barnes (10) identified a series of epizootic host-flea complexes that involved ground squirrel, prairie dog, chipmunk, and wood rat species,
and their fleas. Unlike Kucheruk’s system, however, Barnes’ system was intended
to identify those rodent and flea species most likely involved in the amplification
and geographic spread of plague during epizootics.
LANDSCAPE ECOLOGY STUDIES
Pavlovsky and other Soviet scientists first brought attention to the relationships
between landscapes and the distribution and occurrence of various diseases, including plague (89, 106, 125). These landscape ecology studies continue to provide
insights into the focality of plague and how its spread can be affected by landscape features (4, 95, 126). One recent study hypothesized that the occurrence of
plague epizootics in the Altay mountains, Tuva (Trans-Baikal), Kyzyl Kum desert
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in Uzbekistan, and Caspian lowlands is correlated with medium or high concentration of iron, cobalt, and titanium, and low concentrations of copper, nickel, and
vanadium (126). These field observations were supported by laboratory studies
indicating that manganese, iron, cobalt, nickel, copper, and zinc influenced the
course of Y. pestis infections in three gerbil species (R. opimus, M. meridianus,
and M. tamariscinus) (97). The distribution of foci in China also is reported to be
correlated with calcium- and iron-enriched environments (95).
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CONCLUSIONS AND FUTURE DIRECTIONS
In many respects, research on the natural history of plague presents an excellent
example of how multidisciplinary investigations can enhance our knowledge of
the natural cycles, maintenance, transmission, and focality of zoonotic diseases.
The importance of this research can hardly be questioned, as it has provided critical information for the development of effective plague prevention and control
techniques. And yet this same body of research often has yielded contradictory
results and interpretations that make it difficult to evaluate the relative merits
of different concepts on the dynamics of plague cycles, the occurrence of epizootics and spread of plague, the mechanisms for the interepizootic maintenance of
Y. pestis, the roles of fleas as biological and mechanical vectors, and the distribution
and structure of natural foci. Although such problems are not entirely unexpected,
they point out the need for studies designed to test specific hypotheses on the
above topics. The success of such research likely depends on ongoing support for
long-term studies and collaborations between scientists from many disciplines,
including entomology, ecology, microbiology, molecular biology, mathematical
modeling, geographic information systems, and remote sensing.
The Annual Review of Entomology is online at http://ento.annualreviews.org
LITERATURE CITED
1. Achtman M, Zurth K, Morelli G, Torrea G, Guiyoule A, Carniel E. 1999.
Yersinia pestis, the cause of plague, is a
recently emerged clone of Yersinia pseudotuberculosis. Proc. Natl. Acad. Sci.
USA 96:14043–48
2. Adair DM, Worsham PL, Hill KK,
Klevytska AM, Jackson PJ, et al. 2000.
Diversity in a variable-number tandem
repeat from Yersinia pestis. J. Clin. Microbiol. 38:1516–19
3. Aikimbaev AM, Temiralieva GA. 1990.
About mechanism of plague enzootic. In
Materialy Regional’nogo Soveschania
Protivochumnyh Uchrezhdenii, pp. 10–
12. Kuibyshev, Russ.: Minist. zdravoohr.
SSSR
4. Alekseev EV. 1992. Ecological-geographic characteristics of natural centers of
plague (use of the database of epizootiological investigations). Ekologiya 6:45–
51
5. Anisimov AP. 2002. Factors of Yersinia
pestis providing circulation and persistence of plague pathogen in ecosystems
of natural foci. Mol. Gen. Mikrobiol.
Virusol. 4:3–11
6. Anisimov AP, Lindler LE, Pier GB.
27 Oct 2004 11:37
522
7.
Annu. Rev. Entomol. 2005.50:505-528. Downloaded from arjournals.annualreviews.org
by NEW YORK UNIVERSITY - BOBST LIBRARY on 10/06/05. For personal use only.
8.
9.
10.
11.
12.
13.
14.
15.
AR
GAGE
AR234-EN50-21.tex
AR234-EN50-21.sgm
LaTeX2e(2002/01/18)
P1: GCE
KOSOY
2004. Intraspecific diversity of Yersinia
pestis. Clin. Microbiol Rev. 17:434–64
Atshabar B. 1999. Plague biocenosis as ecological system. In Problemy
Osobo-Opasnih Infektsii, ed. VV Kutirev, 79:36–44. Mikrob Central Antiplague Inst. (Saratov): Slovo Press
Bacot AW, Martin CJ. 1914. Observations on the mechanism of the transmission of plague by fleas. J. Hyg. London
13(Suppl. III):423–39
Baltazard M. 1964. The conservation of
plague in inveterate foci. J. Hyg. Epidemiol. Microbiol. Immunol. 120:409–
21
Barnes AM. 1982. Surveillance and control of bubonic plague in the United
States. Symp. Zool. Soc. London 50:237–
70
Bazanova LP, Maevskii MP. 1996. The
duration of the persistence of plague
microbe in the body of flea Citellophilus tesquorum altaicus. Med. Parasitol. (2):45–48
Bazanova LP, Maevskii MP, Popkov
AF, Galatsevich NF. 2000. Estimation
of the epizootiological role of the flea
Citellophilus tesquorum altaicus in Tuva
plague focus. Sci. J. Cent. Control Res.
Nat. Infect. Dis. 8:67–74
Bazanova LP, Zhovtyi IF, Maevskii MP,
Klimov VT, Popkov AF. 1991. The seasonal dynamics of blocking in the flea
Citellophilus tesquorum altaicus from
the Tuva natural plague focus. Med.
Parazitol. Issue 1 (Jan.):24-26
Bercorvier H, Mollaret HH, Alonso JM,
Brault J, Fanning GR, et al. 1980. Intraand interspecies relatedness of Yersinia
pestis by DNA hybridization and its relationship to Y. pseudotuberculatus. Curr.
Microbiol. 4:225–29
Berlin AL, Borzenkov AK. 1938. Fermentative characterization of Mongolian B. pestis strains. Fermentations of
different carbohydrates, alcohols, and
glycosides. Vestn. Mikrobiol. Epidemiol.
Parazirtol. 17(3–4):215
16. Bibikova VA. 1977. Contemporary
views on the interrelationships between
fleas and the pathogens of human and
animal diseases. Annu. Rev. Entomol.
22:23–32
17. Biggins DE, Kosoy MY. 2001. Disruptions of ecosystems in western North
America due to invasion by plague. J.
Idaho Acad. Sci. 37:62–65
18. Biggins DE, Kosoy MY. 2001. Influences of introduced plague on North
American mammals: implications from
ecology of plague in Asia. J. Mammal.
82:906–16
19. Blanc G. 1956. Une opinion non conformiste sur la mode de transmission de
la peste. Rev. Hyg. Med. Soc. 4:535–62
20. Brubaker RR. 1991. Factors promoting
acute and chronic diseases caused by
yersiniae. Clin. Microbiol. Rev. 4:309–
24
21. Burroughs AL. 1944. The flea Malaraeus telchinum, a vector of P. pestis.
Proc. Soc. Exp. Biol. Med. 55:10–11
22. Burroughs AL. 1947. Sylvatic plague
studies. The vector efficiency of nine
species of fleas compared with Xenopsylla cheopis. J. Hyg. 43:371–96
23. Carniel E. 2003. Evolution of pathogenic
Yersinia, some lights in the dark. Adv.
Exp. Med. Biol. 529:3–12
24. Cavanaugh DC. 1971. Specific effect of
temperature upon transmission of the
plague bacillus by the Oriental rat flea,
Xenopsylla cheopis. Am. J. Trop. Med.
Hyg. 20:264–73
25. Cavanaugh DC, Marshall JD Jr. 1972.
The influence of climate on the seasonal
prevalence of plague in the Republic of
Vietnam. J. Wildl. Dis. 8:85–94
26. Chu MC. 2000. Laboratory Manual of
Plague Diagnostic Tests. Atlanta: Cent.
Dis. Control Prev. 129 pp.
27. Chu MC, Dong XQ, Zhou X, Garon CF.
1998. A cryptic 19-kilobase plasmid associated with U.S. isolates of Yersinia
pestis: a dimer of the 9.5-kilobase plasmid. Am. J. Trop. Med. Hyg. 58:679–86
27 Oct 2004 11:37
AR
AR234-EN50-21.tex
AR234-EN50-21.sgm
LaTeX2e(2002/01/18)
Annu. Rev. Entomol. 2005.50:505-528. Downloaded from arjournals.annualreviews.org
by NEW YORK UNIVERSITY - BOBST LIBRARY on 10/06/05. For personal use only.
NATURAL HISTORY OF PLAGUE
28. Deleted in proof
29. Deleted in proof
30. Cully JF, Barnes AM, Quan TJ, Maupin
G. 1997. Dynamics of plague in a Gunnison’s prairie dog colony complex from
New Mexico. J. Wildl. Dis. 33:706–19
31. Darby C, Hsu JW, Ghori N, Falkow
S. 2002. Plague bacteria biofilm blocks
food intake. Nature 417:243–44
32. Davis RM, Smith RT, Madon MB, SitkoCleugh E. 2002. Flea, rodent, and plague
ecology at Chuchupate Campground,
Ventura County, California. J. Vector
Ecol. 27:107–27
32a. Davis S, Begon M, DeBruyn L, Ageyev
VS, Klassovskiy NL, et al. 2004. Predictive thresholds for plague in Kazakhstan.
Science 304:736–38
33. Degtyareva LV, Labunets NF, Osipova
SP, Shchedrin VI. 1990. The ability
of flea species on common vole from
mountainous Dagestan to transmit and
preserve the causative agent of plague.
Parazitologiya 24(2):106–12
34. Dennis DT. 1998. Plague as an emerging disease. In Emerging Infections, ed.
WM Scheld, WA Craig, JM Hughes,
pp. 169–83. Washington, DC: ASM
Press
35. Dennis DT, Chow CC. 2004. Plague. Pediatr. Infect. Dis. J. 23:69–71
36. Dennis DT, Gage KL. 2003. Plague. In
Infectious Diseases, ed. D Armstrong, J
Cohen, 2(6):1641–48. London: Mosby.
2nd ed.
37. Devignat R. 1951. Varietes del espece
Pasteurella pestis. Nouvelle hypothese.
Bull. World Health Organ. 4:242–63
38. Domaradsky IV. 1999. Is not plague a
“protonosis”? Med. Parazitol. 2:10–13
39. Dong XQ, Lindler LE, Chu MC. 2000.
Complete DNA sequence and analysis
of an emerging cryptic plasmid isolated
from Yersinia pestis. Plasmid 43:144–48
40. Douglas JR, Wheeler CM. 1943. Sylvatic plague studies. II. The fate of Pasteurella pestis in the flea. J. Infect. Dis.
72:18–30
P1: GCE
523
41. Dubyansky MA, Dubyanska LD, Bogatyrev SK. 1992. The relationship between the amount of atmospheric precipitations and the probability for humans to
contract plague in a natural focus of infection. Zh. Mikrobiol. 9–10:46–47
42. Engelthaler DM, Gage KL. 2000.
Quantities of Yersinia pestis in fleas
(Siphonaptera: Pulicidae, Ceratophyllidae, and Hystrichopsyllidae) collected
from areas of known or suspected plague
activity. J. Med. Entomol. 37:422–26
43. Engelthaler DM, Hinnebusch BJ, Rittner CM, Gage KL. 2000. Quantitative
competitive PCR as a method for exploring flea-Yersinia pestis dynamics. Am. J.
Trop. Med. Hyg. 62:552–60
44. Enscore RE, Biggerstaff BJ, Brown TL,
Fulgham RF, Reynolds PJ, et al. 2002.
Modeling relationships between climate
and the frequency of human plague cases
in the southwestern United States, 1960–
1997. Am. J. Trop. Med. Hyg. 66:186–96
45. Ergaliev KH, Pole SB, Stepanov VM.
1990. Blood groups of great gerbils
(Rhombomys opimus Light) as proposed
indicators of population resistance to infections. Genetika 26:103–8
46. Eskey CR, Haas VH. 1940. Plague in the
western part of the United States. Publ.
Health Bull. 254:1–82
47. Fenyuk BK. 1940. Ecological factors of
plague focality. Zool. Zh. 19:349–51
48. Gage KL. 1998. Plague. In Topley and
Wilson’s Microbiology and Microbial Infections.Vol. 3: Bacterial Infections, ed.
L Collier, A Balows, M Sussman, WJ
Hausler, pp. 885–904. London: Arnold.
9th ed.
49. Gage KL. 1999. Plague surveillance. In
Plague Manual, pp. 135–65. Geneva:
World Health Organ.
50. Gage KL, Dennis DT, Orloski KA, Ettestad P, Brown TL, et al. 2000. Cases of human plague associated with exposure to
infected domestic cats. Clin. Infect. Dis.
30:893–900
51. Gage KL, Ostfeld RS, Olson JG. 1995.
27 Oct 2004 11:37
524
52.
Annu. Rev. Entomol. 2005.50:505-528. Downloaded from arjournals.annualreviews.org
by NEW YORK UNIVERSITY - BOBST LIBRARY on 10/06/05. For personal use only.
53.
54.
54a.
55.
56.
57.
58.
AR
GAGE
AR234-EN50-21.tex
AR234-EN50-21.sgm
LaTeX2e(2002/01/18)
P1: GCE
KOSOY
Nonviral vector-borne zoonoses associated with mammals in the United States.
J. Mammal. 76(3):695–715
Gage KL, Thomas RE, Montenieri JA.
1994. The role of predators in the ecology, epidemiology, and surveillance of
plague in the United States. Proc. 16th
Vert. Pest Conf., pp. 200–6. Davis: Univ.
Calif. Press
Gan NV, Voronova GA, Yuzvik LN,
Belyaeva VA. 1990. The capability
of Rhadinopsylla rothschildi and R.
dahurica fleas as vectors of plague
pathogen in Transbaikal natural focus.
Parazitologiya 24(2):151–54
Gayskii NA. 1944. Infection and immunity in hibernating animals. In
Izvestiya Irkutskogo Gosudarstvennogo
protivochumnogo instituta Sibiri i Dalnego Vostoka, Irkutsk. 5:82–123. Irkutsk,
Russ: Irkutsk Antiplague Inst. Siberia
Far East
Girard JM, Wagner DM, Vogler AJ, Keys
C, Allender CJ, et al. 2004. Differential plague-transmission dynamics determine Yersinia pestis population genetic structure on local, regional, and
global scales. Proc. Natl. Acad. Sci. USA
101:8408–13
Golov DA, Ioff AG. 1928. On the question of the role of the rodent fleas in
the southeastern part of the USSR and
the epidemiology of plague. Proc. 1st
All-Russian Anti-Plague Conf. Saratov,
pp. 102–5. Saratov, Russ: Mikrob Central Antiplague Inst.
Gorschkov OV, Savostina EP, Popov
YA, Plotnikov OP, Vinogradova NA,
Solodovnikov NS. 2000. Genotyping
Yersinia pestis strains from various natural foci. Mol. Gen. Mikrobiol. Virusol.
3:12–17
Gratz NG. 1999. Rodent reservoirs and
flea vectors of natural foci of plague.
In Plague Manual, pp. 63–96. Geneva:
World Health Organ.
Gubareva NP, Akiev AK, Zemelman
BM, Abdurakhmanov GA. 1976. The ef-
59.
60.
61.
62.
63.
64.
65.
66.
67.
fect of some factors of the block formation in fleas Ceratophyllus tesquorum
and Neopsylla setosa. Parazitologiya
10(4):315–19
Guiyoule A, Grimont F, Iteman I, Grimont PAD, Lefevre M, Carniel E. 1994.
Plague pandemics investigated by ribotyping of Yersinia pestis strains. J. Clin.
Microbiol. 32:633–41
Hinnebusch BJ. 1997. Bubonic plague:
a molecular genetic case history of the
emergence of an infectious disease. J.
Mol. Med. 75:645–52
Hinnebusch BJ, Fischer ER, Schwan
TG. 1998. Evaluation of the role of
the Yersinia pestis plasminogen activator and other plasmid-encoded factors in
temperature-dependent blockage of the
flea. J. Infect. Dis. 178:1406–15
Hinnebusch BJ, Gage KL, Schwan TG.
1998. Estimation of vector infectivity
rates for plague by means of a standard
curve-based competitive PCR method to
quantify Yersinia pestis in fleas. Am. J.
Trop. Med. Hyg. 58:562–69
Hinnebusch BJ, Perry RD, Schwan TG.
1996. Role of the Yersinia pestis hemin
storage (hms) locus in the transmission
of plague by fleas. Science 273:367–70
Hinnebusch BJ, Rudolph AE, Cherepenov P, Dixon JE, Schwan TG, Forsberg
A. 2002. Role of Yersinia murine toxin in
survival of Yersinia pestis in the midgut
of the flea vector. Science 296:733–
35
Holdenried R. 1952. Sylvatic plague
studies. VII. Plague transmission potentials of the fleas Diamanus montanus and
Polygenis gwyni compared with Xenopsylla cheopis. J. Infect. Dis. 90:131–
40
Holdenried R, Morlan HB. 1955. Plagueinfected fleas from northern New Mexico
wild rodents. J. Infect. Dis. 96:133–37
Holdenried R, Quan SF. 1956. Susceptibility of New Mexico rodents to experimental plague. Publ. Health Rep. 71:
979–84
27 Oct 2004 11:37
AR
AR234-EN50-21.tex
AR234-EN50-21.sgm
LaTeX2e(2002/01/18)
Annu. Rev. Entomol. 2005.50:505-528. Downloaded from arjournals.annualreviews.org
by NEW YORK UNIVERSITY - BOBST LIBRARY on 10/06/05. For personal use only.
NATURAL HISTORY OF PLAGUE
68. Huang X, Chu MC, Engelthaler DM,
Lindler LE. 2002. Genotyping of a
homogeneous group of Yersinia pestis
strains isolated in the United States. J.
Clin. Microbiol. 40:1164–73
69. Hubbert WT, Goldenberg MI. 1970. Natural resistance to plague: genetic basis in
the vole (Microtus californicus). Am. J.
Trop. Med. Hyg. 19:1015–19
70. Inglesby TV, Dennis DT, Henderson DA,
Bartlett JG, Ascher MS, et al. 2000.
Plague as a biological weapon. JAMA
283:2281–90
71. Isin ZM, Suleimenov BM. 1987. Comparative investigation of PMN leukocyte
antimicrobial potential I animals of different species susceptibility to the plague
agent. J. Hyg. Epidemiol. Microbiol. Immunol. 31:307–12
71a. Jarrett CO, Deak E, Isherwood KE, Oyston PC, Fischer ER, et al. 2004. Transmission of Yersinia pestis from an infectious biofilm in the flea vector. J. Infect.
Dis. 190:783–92
72. Kalabukhov NL. 1965. The structure and
dynamics of natural foci of plague. J.
Hyg. Epidemiol. Microbiol. 9:147–59
73. Kartman L. 1957. The concept of vector efficiency in experimental studies of
plague. Exp. Parasitol. 6:599–609
74. Kartman L. 1969. Effect of differences
in ambient temperature upon the fate of
Pasteurella pestis in Xenopsylla cheopis.
Trans. R. Soc. Trop. Med. Hyg. 63:71–75
75. Kartman L, Prince FM. 1956. Studies on
Pasteurella pestis in fleas. V. The experimental plague-vector efficiency of wild
rodent fleas compared with Xenopsylla
cheopis, together with observations on
the influence of temperature. Am. J. Trop.
Med. Hyg. 5:1058–70
76. Kartman L, Prince FM, Quan SF. 1958.
Studies of Pasteurella pestis in fleas
VII. The plague-vector efficiency of
Hystrichopsylla linsdalei compared with
Xenopsylla cheopis under experimental
conditions. J. Trop. Med. Hyg. 7:317–22
77. Kartman L, Prince FM, Quan SF, Stark
78.
79.
80.
81.
82.
83.
84.
85.
86.
87.
88.
P1: GCE
525
HE. 1958. New knowledge of the ecology of sylvatic plague. Ann. NY Acad.
Sci. 70:668–711
Kartman L, Quan SF, Lechleitner RR.
1962. Die-off of a Gunnison’s prairie dog
colony in central Colorado II. Retrospective determination of plague infection in
flea vectors, rodents and man. Zoonoses
Res. 1:201–24
Kartman L, Quan SF, Stark HE. 1962.
Ecological studies of wild rodent plague
in the San Francisco Bay Area of California. VII. Effects of plague in nature
on Microtus californicus and other wild
rodents. Zoonoses Res. 1:99–119
Keeling MJ, Gilligan CA. 2000. Bubonic
plague: a metapopulation model of a
zoonosis. Proc. R. Soc. London B 267:
2219–30
Keeling MJ, Gilligan CA. 2000.
Metapopulation dynamics of bubonic
plague. Nature 407:903–6
Klevytska A, Price LB, Schupp JM,
Worsham PL, Wong J, Keim P. 2001.
Identification and characterization of
variable-number tandem repeats in the
Yersinia pestis genome. J. Clin. Microbiol. 39:3179–85
Deleted in proof
Korzun VM, Nikitin AI. 1997. Asymmetry of chaetae in fleas Citellophilus
tesquorum as a possible marker of their
capacity for blocking. Med. Parazitol.
(1):34–36
Kozakevich VP. 1969. Dependence of
susceptibility of little susliks to plague on
their physiological status. Probl. Osoboopasnih Infekt. 5(9):74–80
Kozlov M. 1979. Plague. Natural Focality, Epizootiology, and Epidemic Manifestations. Moscow: Meditsina. 192 pp.
Kozlov MP. 1983. Epizootic process of
infections with natural focality from the
standpoint of systems theory. Zh. Mikrobiol. (10):8–13
Krylova KT, Shilova ES. 1970. Epizootiological significance of ecology of
large-toothed suslik in northern pre-Ural.
27 Oct 2004 11:37
526
89.
Annu. Rev. Entomol. 2005.50:505-528. Downloaded from arjournals.annualreviews.org
by NEW YORK UNIVERSITY - BOBST LIBRARY on 10/06/05. For personal use only.
90.
91.
92.
93.
94.
95.
96.
97.
98.
99.
AR
GAGE
AR234-EN50-21.tex
AR234-EN50-21.sgm
LaTeX2e(2002/01/18)
P1: GCE
KOSOY
Probl. Osobo-opasnih Infekt. 4(14):172–
77
Kucheruk VV. 1960. Experience in classification of natural foci of plague in Holarctic Eurasia. Med. Parazitol. 28:5–15
Kucheruk VV. 1965. Paleogenesis of
plague natural foci in connection with
history of rodent fauna. In Fauna i Ekologia Grizunov, 7:5–86. Moscow: Izdatelstvo MGU
Lavrovskii AA, Varshavskii SN. 1970.
Some topical problems in plague natural focality. Probl. Osobo-opasnih Infekt.
pp. 13–23
Levi MI. 1962. Classification of the
varieties of the plague bacillus. In
Tezisy Dokladov Nauchnoi Konferentsii
po Prirodnoi Ochagovosti Chumy i Tularemii, pp. 72–74. Rostov, Russ.
Levy CE, Gage KL. 1999. Plague in the
United States 1995–1996, with a brief
review of the disease and its prevention.
Infect. Med. 16:54–64
Litvin VY. 1997. Mechanisms of the stable preservation of Yersinia pestis in the
environment (new facts and hypotheses).
Zh. Mikrobiol. (4):26–31
Liu Y, Tan J, Shen E, eds. 2000. The
Atlas of Plague and Its Environment in
the People’s Republic of China. Beijing:
Inst. Geographical Sci. Nat. Res., Chin.
Acad. Sci. 201 pp.
Meyer KF. 1942. The ecology of plague.
Medicine 21:143–74
Mezentsev VM, Rotshild EV, Medzykhovsky GA, Grazhdanov AK. 2000. Experimental study of the influence of trace
elements on plague infection. Zh. Mikrobiol. Moscow (1):41–45
Mollaret HH. 1963. Conservation experimentale de la peste dans le sol. Bull. Soc.
Pathol. Exot.. 56:1168–82
Motin VL, Georgescu AM, Elliott JM,
Hu P, Worsham PL, et al. 2002. Genetic
variability of Yersinia pestis isolates as
predicted by PCR-based IS100 genotyping and analysis of structural genes
encoding glycerol-3-phosphate dehy-
100.
101.
102.
103.
104.
105.
106.
107.
108.
109.
drogenase (glpD). J. Bacteriol. 184:
1019–27
Nekipelov NV. 1959. Rodents as carriers of plague in Mongolia. In Izvestiya
Irkutskogo gosudarstvennogo protivochumnogo instituta Sibiri i Dalnego Vostoka, Irkutsk. Irkutsk Antiplague Inst.
Siberia Far East. Irkutsk, Russ. Monogr.
22:17–71
Nelson BC, Smith CR. 1980. Ecology
of sylvatic plague in lava caves at Lava
Beds National Monument, California. In
Fleas, ed. R Traub, H Starcke, pp. 273–
75. Rotterdam: AA Balkema
Nersesov V, Tsikhistavi G. 1997. On
the mechanism of existence of Yersinia
pestis in nature. Zh. Mikrobiol. (1):102–6
Nikul’shin SV, Onatskaia TG, Lukanina LM, Bondarenko AL. 1992. Associations of the soil amoeba Hartmanella
rhysodes with the bacterial causative
agents of plague and pseudotuberculosis
in an experiment. Zh. Mikrobiol. 9–10:2–
5
Pak GY, Stepanov VM, Satybaldiev
NA, Bakanurskaya TL, Aniskin GP.
1990. On the role of bacteriophages in
self-regulation of plague epizootic. Zh.
Mikrobiol. (9):97–100
Parmenter RR, Yadav EP, Parmenter CA,
Ettestad P, Gage KL. 1999. Incidence of
plague associated with increased winterspring precipitation in New Mexico,
USA. Am. J. Trop. Med. Hyg. 61:814–
21
Pavlovsky EN. 1966. Natural Nidality of
Transmissible Diseases. Chicago: Univ.
Illinois Press. 261 pp.
Perry RD, Bearden SW, Fetherston JD.
2001. Iron and heme acquisition and storage systems of Yersinia pestis. Rec. Res.
Dev. Microbiol. 5:13–27
Perry RD, Fetherston JD. 1997. Yersinia
pestis: etiologic agent of plague. Clin.
Microbiol. Rev. 10:35–66
Petrov VS. 1959. Natural foci of plague
in Eurasia and the principles of their
typification. In Trudi Sredneaziatskogo
27 Oct 2004 11:37
AR
AR234-EN50-21.tex
AR234-EN50-21.sgm
LaTeX2e(2002/01/18)
NATURAL HISTORY OF PLAGUE
Annu. Rev. Entomol. 2005.50:505-528. Downloaded from arjournals.annualreviews.org
by NEW YORK UNIVERSITY - BOBST LIBRARY on 10/06/05. For personal use only.
110.
111.
112.
113.
114.
115.
116.
117.
118.
Protivochumnogo Instituta,
Almaty.
Monogr. 6:3–12. Almaty, Kazakhstan.
Petrunina OM. 1951. A course of plague
infection in great gerbils (Rhombomys
opimus Licht.) under experimental
inoculation. In Trudy Sredneaziatskogo
Nauchno-Issledovatel’skogo Protivochumnogo Instituta, Alma-Ata. Monogr.
1:17–25. Alma-Ata (Almaty), Kazakhstan.
Poland J, Barnes A. 1979. Plague. In
CRC Handbook Series in Zoonoses, Section A: Bacterial, Rickettsial, and Mycotic Diseases, Vol. 1., ed. JH Steele, H
Stoenner, W Kaplan, pp. 515–97. Boca
Raton, FL: CRC Press
Poland J, Quan TJ, Barnes AM. 1994.
Plague. In CRC Handbook Series in
Zoonoses. Section A: Bacterial, Rickettsial, and Mycotic Diseases, ed. GW
Beran, pp. 93–112. Boca Raton, FL:
CRC Press
Pollitzer R. 1954. Plague. World Health
Organization Monograph Series No. 22.
Geneva: World Health Organ. 698 pp.
Pollitzer R. 1960. A review of recent literature on plague. Bull. World Health.
Organ. 23:313–400
Pollitzer R, Meyer KF. 1961. The ecology of plague. In Studies of Disease
Ecology,ed. JF May, pp. 433–501. New
York: Hafner
Prentice MB, James KD, Parkhill J,
Baker SG, Stevens K, et al. 2001.
Yersinia pestis pFRa shows biovarspecific differences and recent common ancestry with a Salmonella enterica serovar typhi plasmid. J. Bacteriol.
183:2586–94
Pushkareva VI. 2003. Experimental evaluation of interactions between Yersinia
pestis EV and soil infusoria and the
possibility of the prolonged preservation
of bacteria in the protozoan cysts. Zh.
Mikrobiol. 4:40–44
Quan SF, Burroughs AL, Holdenried R,
Meyer KF. 1953. Studies on the prevention of experimental plague epizootics
119.
120.
121.
122.
123.
124.
125.
126.
127.
P1: GCE
527
instituted among mice by infected fleas.
Atti VI Congr. Int. Microbiol. Roma
5:XVI:537–40
Quan SF, Kartman L. 1956. The resistance of Microtus and Peromyscus to infection by Pasteurella pestis. Trans. R.
Soc. Trop. Med. Hyg. 50:104–5
Quan SF, Kartman L. 1962. Ecological
studies of wild rodent plague in the San
Francisco Bay Area of California. VIII.
Susceptibility of wild rodents to experimental plague infection. Zoonoses Res.
1:121–44
Quan TJ, Barnes AM, Carter LG,
Tsuchiya KR. 1985. Experimental
plague in rock squirrels, Spermophilus
variegatus (Erxleben). J. Wildl. Dis. 21:
205–10
Rall YuM. 1965. Natural Focality and
Epizootiology of Plague. Moscow: Medgiz. 338 pp.
Rivkus Y, Ostrovskii I, Melnikov I, Dyatlov A. 1973. On sensitivity to plague
in Rhombomys opimus from the northern Kizil-Kum. Probl. Osobo-opasnih
Infekt. Monogr. 30(2):48–58. Saratov,
Russ.
Rivkus YZ, Mitropolsky OV, Bochkaroff
VM, Blummer AG, Bochkaroff SV.
1993. Desert vegetation as a possible
component in plague parasitocoenosis.
Bull. Mosk. Obschestva Ispyt. Prirody.
98:3–13
Rotshild EV. 1978. Spatial Structure of
a Natural Center of Plague and Methods of Studying It. Moscow: Izdatelstvo
MGU. 192 pp.
Rotshild EV. 2001. Relationship between infectious diseases and concentration of trace metals in the environment
and periodic law. Uspehi Sovrem. Biol.
121:251–65
Serzhan OS, Ageyev VS. 2000. Geographical distribution and host complexes of plague-infected fleas in
relation to some problems of paleogenesis of plague enzootics. In Karantinye i
Zoonoznye Infektsii v Kazakhstane, ed.
27 Oct 2004 11:37
528
128.
Annu. Rev. Entomol. 2005.50:505-528. Downloaded from arjournals.annualreviews.org
by NEW YORK UNIVERSITY - BOBST LIBRARY on 10/06/05. For personal use only.
129.
130.
131.
132.
133.
134.
AR
GAGE
AR234-EN50-21.tex
AR234-EN50-21.sgm
LaTeX2e(2002/01/18)
P1: GCE
KOSOY
BB Atshabar, 2:183–92. Almaty: Kazakhskii Protivochumnyi Inst.
Sharets AS, Berendyev SA, Krasnikova
LV, Tristan DF. 1958. Effectiveness of
the one shot marmot control. In Trudy
Sredneaziatskogo Protivochumnogo Instituta. Monogr. 4:145–47. Almaty,
Kazakhstan
Stapp P, Antolin MF, Ball M. 2004.
Patterns of extinction in prairie-dog
metapopulations: plague outbreaks follow El Nino events. Front. Ecol. Environ.
2:235–40
Stepanov VM. 1975. Nutrition Factors
and Their Role in Manifestation of Virulence and Immunogenicity of Plague
Pathogen. Saratov, Russ.: Mikrob. Central Antiplague Inst. 285 pp.
Suchkov IG, Khudiakov IV, Emel’ianenko EN, Levi MI, Pushkareva VI,
et al. 1997. The possibility of preserving
the causative agent of plague in soil in
resting (nonculturable) form. Zh. Mikrobiol. Epidemiol. Immunobiol. 4:42–
46
Suntsov VV, Suntsova NI. 2000. Ecological aspects of evolution of the plague
microbe Yersinia pestis and the genesis
of natural foci. Biol. Bull. 27:541–42
Thomas RE, Barnes AM, Quan TJ, Beard
ML, Carter LG, Hopla CE. 1988. Susceptibility to Yersinia pestis in the northern grasshopper mouse (Onychomys
leucogaster). J. Wildl. Dis. 24:327–33
Tikhomirova MM. 1934. The midday
gerbil, Meriones meridianus Pall., carrier of plague in the sandy areas of the
southern Volga-Ural steppes. Rev. Microbiol. Saratov. 13:89–102
135. Titball RW, Hill J, Lawton DG, Brown
KA. 2003. Yersinia pestis and plague.
Biochem. Soc. Trans. 31(Pt. 1):104–7
136. Trebesius K, Harmsen D, Rakin A,
Schmelz J, Heesemann J. 1998. Development of rRNA-targeted PCR and
in situ hybridization with fluorescently
labelled oligonucleotides for detection
of Yersinia species. J. Clin. Microbiol.
36:2557–64
136a. Trudeau KM, Britten HB, Restani M.
2004. Sylatic plague reduces genetic
variability in black-tailed prairie dogs. J.
Wildl. Dis. 40:205–11
137. Tumanskii VM. 1957. Classification of
the varieties of P. pestis. Zh. Mikrobiol.
28:3
138. Tumanskii VM. 1958. Mikrobiologiia
Chumy. Moscow: Medgiz. 2nd ed.
139. Deleted in proof
140. Voronova GA. 1989. Enhanced blocking
capability of plague microbe in the body
of flea. Parazitologiya 23(5):427–29
141. Williams JE, Cavanaugh DC. 1983.
Chronic infections in laboratory rodents
from inoculation of nonencapsulated
plague bacilli (Yersinia pestis). Experentia 39:408–9
142. Williams JE, Harrison DN, Cavanaugh
DC. 1975. Cryptic infection of rats with
non-encapsulated variants of Yersinia
pestis. Trans. R. Soc. Trop. Med. Hyg.
69:171–72
143. World Health Organization. 2003. Human plague in 2000 and 2001. Wkly. Epidemiol. Rec. 78:129–36
144. Zabolotny DK. 1915. Pulmonary Plague
in 1910–1911. Accounts of the Russian
Scientific Expedition. Petrograd, Russ.
P1: JRX
October 28, 2004
21:8
Annual Reviews
AR234-FM
Annual Review of Entomology
Volume 50, 2005
Annu. Rev. Entomol. 2005.50:505-528. Downloaded from arjournals.annualreviews.org
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CONTENTS
BIOLOGY AND MANAGEMENT OF INSECT PESTS IN NORTH AMERICAN
INTENSIVELY MANAGED HARDWOOD FOREST SYSTEMS,
David R. Coyle, T. Evan Nebeker, Elwood R. Hart,
and William J. Mattson
THE EVOLUTION OF COTTON PEST MANAGEMENT PRACTICES IN
CHINA, K.M. Wu and Y.Y. Guo
MOSQUITO BEHAVIOR AND VECTOR CONTROL, Helen Pates
and Christopher Curtis
1
31
53
THE GENETICS AND GENOMICS OF THE SILKWORM, BOMBYX MORI,
Marian R. Goldsmith, Toru Shimada, and Hiroaki Abe
TSETSE GENETICS: CONTRIBUTIONS TO BIOLOGY, SYSTEMATICS, AND
CONTROL OF TSETSE FLIES, R.H. Gooding and E.S. Krafsur
MECHANISMS OF HOPPERBURN: AN OVERVIEW OF INSECT TAXONOMY,
BEHAVIOR, AND PHYSIOLOGY, Elaine A. Backus, Miguel S. Serrano,
and Christopher M. Ranger
71
101
125
FECAL RESIDUES OF VETERINARY PARASITICIDES: NONTARGET
EFFECTS IN THE PASTURE ENVIRONMENT, Kevin D. Floate,
Keith G. Wardhaugh, Alistair B.A. Boxall, and Thomas N. Sherratt
153
THE MEVALONATE PATHWAY AND THE SYNTHESIS OF JUVENILE
HORMONE IN INSECTS, Xavier Bellés, David Martı́n,
and Maria-Dolors Piulachs
181
FOLSOMIA CANDIDA (COLLEMBOLA): A “STANDARD” SOIL
ARTHROPOD, Michelle T. Fountain and Steve P. Hopkin
CHEMICAL ECOLOGY OF LOCUSTS AND RELATED ACRIDIDS,
201
Ahmed Hassanali, Peter G.N. Njagi, and Magzoub Omer Bashir
223
THYSANOPTERA: DIVERSITY AND INTERACTIONS, Laurence A. Mound
EFFECTS OF PLANTS GENETICALLY MODIFIED FOR INSECT
RESISTANCE ON NONTARGET ORGANISMS, Maureen O’Callaghan,
Travis R. Glare, Elisabeth P.J. Burgess, and Louise A. Malone
247
271
vii
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October 28, 2004
viii
21:8
Annual Reviews
AR234-FM
CONTENTS
INVASIVE PHYTOPHAGOUS PESTS ARISING THROUGH A RECENT
TROPICAL EVOLUTIONARY RADIATION: THE BACTROCERA DORSALIS
COMPLEX OF FRUIT FLIES, Anthony R. Clarke, Karen F. Armstrong,
Amy E. Carmichael, John R. Milne, S. Raghu, George K. Roderick,
and David K. Yeates
293
PHEROMONE-MEDIATED AGGREGATION IN NONSOCIAL ARTHROPODS:
AN EVOLUTIONARY ECOLOGICAL PERSPECTIVE, Bregje Wertheim,
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by NEW YORK UNIVERSITY - BOBST LIBRARY on 10/06/05. For personal use only.
Erik-Jan A. van Baalen, Marcel Dicke, and Louise E.M. Vet
EGG DUMPING IN INSECTS, Douglas W. Tallamy
ECOLOGICAL, BEHAVIORAL, AND BIOCHEMICAL ASPECTS OF INSECT
HYDROCARBONS, Ralph W. Howard and Gary J. Blomquist
THE EVOLUTION OF MALE TRAITS IN SOCIAL INSECTS,
Jacobus J. Boomsma, Boris Baer, and Jürgen Heinze
321
347
371
395
EVOLUTIONARY AND MECHANISTIC THEORIES OF AGING,
Kimberly A. Hughes and Rose M. Reynolds
421
TYRAMINE AND OCTOPAMINE: RULING BEHAVIOR AND METABOLISM,
Thomas Roeder
447
ECOLOGY OF INTERACTIONS BETWEEN WEEDS AND ARTHROPODS,
Robert F. Norris and Marcos Kogan
NATURAL HISTORY OF PLAGUE: PERSPECTIVES FROM MORE THAN A
CENTURY OF RESEARCH, Kenneth L. Gage and Michael Y. Kosoy
EVOLUTIONARY ECOLOGY OF INSECT IMMUNE DEFENSES,
Paul Schmid-Hempel
SYSTEMATICS, EVOLUTION, AND BIOLOGY OF SCELIONID AND
PLATYGASTRID WASPS, A.D. Austin, N.F. Johnson, and M. Dowton
479
505
529
553
INDEXES
Subject Index
Cumulative Index of Contributing Authors, Volumes 41–50
Cumulative Index of Chapter Titles, Volumes 41–50
ERRATA
An online log of corrections to Annual Review of Entomology
chapters may be found at http://ento.annualreviews.org/errata.shtml
583
611
616